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Research Papers

Fibril Microstructure Affects Strain Transmission Within Collagen Extracellular Matrices

[+] Author and Article Information
Blayne A. Roeder

Weldon School of Biomedical Engineering, Purdue University, 206 South Martin Jischke Drive, West Lafayette, IN 47907-2032; School of Mechanical Engineering, Purdue University, 585 Purdue Mall, West Lafayette, IN 47907-2088blayne_roeder@yahoo.comSchool of Mechanical Engineering, Purdue University, 585 Purdue Mall, West Lafayette, IN 47907-2088; Weldon School of Biomedical Engineering, Purdue University, 206 South Martin Jischke Drive, West Lafayette, IN 47907-2032blayne_roeder@yahoo.comWeldon School of Biomedical Engineering, Purdue University, 206 South Martin Jischke Drive, West Lafayette, IN 47907-2032; Department of Basic Medical Sciences, Purdue University, 625 Harrison Street, West Lafayette, IN 47907-2026blayne_roeder@yahoo.com

Klod Kokini

Weldon School of Biomedical Engineering, Purdue University, 206 South Martin Jischke Drive, West Lafayette, IN 47907-2032; School of Mechanical Engineering, Purdue University, 585 Purdue Mall, West Lafayette, IN 47907-2088kokini@purdue.eduSchool of Mechanical Engineering, Purdue University, 585 Purdue Mall, West Lafayette, IN 47907-2088; Weldon School of Biomedical Engineering, Purdue University, 206 South Martin Jischke Drive, West Lafayette, IN 47907-2032kokini@purdue.eduWeldon School of Biomedical Engineering, Purdue University, 206 South Martin Jischke Drive, West Lafayette, IN 47907-2032; Department of Basic Medical Sciences, Purdue University, 625 Harrison Street, West Lafayette, IN 47907-2026kokini@purdue.edu

Sherry L. Voytik-Harbin1

Weldon School of Biomedical Engineering, Purdue University, 206 South Martin Jischke Drive, West Lafayette, IN 47907-2032; School of Mechanical Engineering, Purdue University, 585 Purdue Mall, West Lafayette, IN 47907-2088harbins@purdue.eduSchool of Mechanical Engineering, Purdue University, 585 Purdue Mall, West Lafayette, IN 47907-2088; Weldon School of Biomedical Engineering, Purdue University, 206 South Martin Jischke Drive, West Lafayette, IN 47907-2032harbins@purdue.eduWeldon School of Biomedical Engineering, Purdue University, 206 South Martin Jischke Drive, West Lafayette, IN 47907-2032; Department of Basic Medical Sciences, Purdue University, 625 Harrison Street, West Lafayette, IN 47907-2026harbins@purdue.edu

1

Corresponding author.

J Biomech Eng 131(3), 031004 (Jan 05, 2009) (11 pages) doi:10.1115/1.3005331 History: Received February 09, 2008; Revised September 22, 2008; Published January 05, 2009

The next generation of medical devices and engineered tissues will require development of scaffolds that mimic the structural and functional properties of the extracellular matrix (ECM) component of tissues. Unfortunately, little is known regarding how ECM microstructure participates in the transmission of mechanical load information from a global (tissue or construct) level to a level local to the resident cells ultimately initiating relevant mechanotransduction pathways. In this study, the transmission of mechanical strains at various functional levels was determined for three-dimensional (3D) collagen ECMs that differed in fibril microstructure. Microstructural properties of collagen ECMs (e.g., fibril density, fibril length, and fibril diameter) were systematically varied by altering in vitro polymerization conditions. Multiscale images of the 3D ECM macro- and microstructure were acquired during uniaxial tensile loading. These images provided the basis for quantification and correlation of strains at global and local levels. Results showed that collagen fibril microstructure was a critical determinant of the 3D global and local strain behaviors. Specifically, an increase in collagen fibril density reduced transverse strains in both width and thickness directions at both global and local levels. Similarly, collagen ECMs characterized by increased fibril length and decreased fibril diameter exhibited increased strain in width and thickness directions in response to loading. While extensional strains measured globally were equivalent to applied strains, extensional strains measured locally consistently underpredicted applied strain levels. These studies demonstrate that regulation of collagen fibril microstructure provides a means to control the 3D strain response and strain transfer properties of collagen-based ECMs.

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Copyright © 2009 by American Society of Mechanical Engineers
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References

Figures

Grahic Jump Location
Figure 1

Characteristic 3D global and local strain responses for a collagen ECM polymerized at a collagen concentration of 2.0 mg/ml and pH 7.4. Globally, applied tensile strain (ε11,applied) resulted in an extension of the gauge section ((a) (ε11,global)) that was equivalent to the applied strain as well as substantial compressions in width ((b) (ε22,global)) and thickness ((c) (ε33,global)) directions. Locally, applied tensile strain resulted in a local extensional strain ((d) (ε11,local)) that underpredicted applied values and substantial decreases in width ((g) (ε22,local)) and thickness ((i) (ε33,local)) strains that mimic those measured globally. No significant shear strains were measured locally ((e), (f), and (h)).

Grahic Jump Location
Figure 2

A series of 2D projections of 3D confocal reflection images showing the microstructure-dependent deformation experienced locally by component collagen fibrils. Deformation of collagen fibrils within ECM constructs of increasing fibril density (polymerized at increasing collagen concentration) is shown at designated strain levels. The arrow designates fibril buckling event.

Grahic Jump Location
Figure 3

A series of 2D projections of 3D confocal reflection images showing the microstructure-dependent deformation experienced locally by component collagen fibrils. Deformation of collagen fibrils within ECM constructs polymerized at pH 6.0 and pH 9.0 is shown at designated strain levels.

Grahic Jump Location
Figure 4

The effect of fibril density ((a) collagen concentration) and fibril aspect ratio ((b) polymerization pH) on the relationship between strains measured globally in the 1-direction (loading) and 2-direction (width). Global width strains (for a given ε11,global) decreased as a function of increasing fibril density and decreasing fibril aspect ratio (n=5 for each collagen ECM microstructure; p<0.05).

Grahic Jump Location
Figure 5

The effect of fibril density ((a) collagen concentration) and fibril aspect ratio ((b)polymerization pH) on the relationship between strains measured globally in the 1-direction (loading) and 3-direction (thickness). Global thickness strains (for a given ε11,global) decreased as a function of increasing fibril density and decreasing fibril aspect ratio (n=5 for each collagen ECM microstructure; p<0.05).

Grahic Jump Location
Figure 6

The effect of fibril density ((a) collagen concentration) and fibril aspect ratio ((b) polymerization pH) on the relationship between strains measured locally in the 1-direction (loading) and 2-direction (width). Local width strains (for a given ε11,local) decreased as a function of increasing fibril density and decreasing fibril aspect ratio (n=5 for each collagen ECM microstructure; p<0.05).

Grahic Jump Location
Figure 7

The effect of fibril density ((a) collagen concentration) and fibril aspect ratio ((b) polymerization pH) on the relationship between locally measured strain in the 1-direction (loading) and 3-direction (thickness). Local thickness strains (for a given ε11,local) decreased as a function of increasing fibril density and decreasing fibril aspect ratio (n=5 for each collagen ECM microstructure; p<0.05).

Grahic Jump Location
Figure 8

The effect of fibril density ((a) collagen concentration) and fibril aspect ratio ((b) polymerization pH) on the relationship between applied and globally measured strains in the 1-direction (loading direction). Variation of polymerization conditions did not significantly alter the transfer of applied extensional strains to those measured globally (n=5 for each collagen ECM microstructure; p>0.05).

Grahic Jump Location
Figure 9

The effect of fibril density ((a) collagen concentration) and fibril aspect ratio ((b) polymerization pH) on the relationship between globally and locally measured strains in the 1-direction (loading direction). At higher strain levels, local extensional strain measurements underpredicted those measured globally regardless of microstructure (n=5 for each collagen ECM microstructure).

Grahic Jump Location
Figure 10

The effect of fibril density ((a) collagen concentration) and fibril aspect ratio ((b) polymerization pH) on the relationship between globally and locally measured strains in the 2-direction (width direction; n=5 for each collagen ECM microstructure)

Grahic Jump Location
Figure 11

The effect of fibril density ((a) collagen concentration) and fibril aspect ratio ((b) polymerization pH) on the relationship between globally and locally measured strains in the 3-direction (thickness direction). Collagen ECMs produced with reduced fibril aspect ratios had a reduced amount of local strain for an equivalent amount of global strain (n=5 for each collagen ECM microstructure; p<0.05).

Grahic Jump Location
Figure 12

Two simple model systems representing different collagen ECM microstructures in which collagen fibrils are modeled as inextensible elements with hinge connections. As shown here, maximum extensional strain ε11 is dependent on the organization of component collagen fibrils.

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